The PAF1 complex is involved in embryonic epidermal morphogenesis in Caenorhabditis elegans

Developmental Biology

Volumn 391, Issue 1, 2014, Pages 43-53

  Kubota, Yukihiko ^a   Tsuyama, Kenji ^a   Takabayashi, Yusuke ^a   Haruta, Nami ^a   Maruyama, Rika ^b,c   Iida, Naoko ^b,d   Sugimoto, Asako ^a,b  

^a TOHOKU UNIVERSITY   (Japan)

^b RIKEN Center for Biosystems Dynamics Research   (Japan)

^c UNIVERSITY OF ALBERTA   (Canada)

^d NATIONAL INSTITUTE OF GENETICS   (Japan)

Author keywords

Caenorhabditis elegans; Embryogenesis; Epidermal morphogenesis; PAF1 complex

Indexed keywords

CAENORHABDITIS ELEGANS PROTEIN; GREEN FLUORESCENT PROTEIN; POLYMERASE ASSOCIATED FACTOR 1 COMPLEX; PROTEIN CDC 73; PROTEIN LEO 1; PROTEIN PAFO 1; PROTEIN RTFO 1; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CAENORHABDITIS ELEGANS; CELL COUNT; CELL FATE; CELL NUCLEUS; CELL SHAPE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CTR 9 GENE; EMBRYO DEATH; EMBRYO DEVELOPMENT; EMBRYONIC EPIDERMAL MORPHOGENESIS; EPIDERMIS CELL; GENE; GENE DELETION; LEO 1 GENE; LETHALITY; MORPHOGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; ORTHOLOGY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RNA INTERFERENCE; SKIN DEFECT;

ANIMALIA; CAENORHABDITIS ELEGANS;

CAENORHABDITIS ELEGANS; EMBRYOGENESIS; EPIDERMAL MORPHOGENESIS; PAF1 COMPLEX;

ACTINS; ALLELES; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL NUCLEUS; CHROMATIN; EPIDERMIS; GENE DELETION; GREEN FLUORESCENT PROTEINS; MORPHOGENESIS; MUTATION; PHENOTYPE; PROMOTER REGIONS, GENETIC; RNA INTERFERENCE; TIME FACTORS;

EID: 84899937257     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2014.04.002     Document Type: Article

References (68)

1. Adelman K., Wei W., Ardehali M.B., Werner J., Zhu B., Reinberg D., Lis J.T. Drosophila Paf1 modulates chromatin structure at actively transcribed genes. Mol. Cell. Biol. 2006, 26:250-260.
2. Akanuma T., Koshida S., Kawamura A., Kishimoto Y., Takada S. Paf1 complex homologues are required for Notch-regulated transcription during somite segmentation. EMBO Rep. 2007, 8:858-863.
3. Bai X., Kim J., Yang Z., Jurynec M.J., Akie T.E., Lee J., LeBlanc J., Sessa A., Jiang H., DiBiase A., Zhou Y., Grunwald D.J., Lin S., Cantor A.B., Orkin S.H., Zon L.I. TIF1gamma controls erythroid cell fate by regulating transcription elongation. Cell 2010, 142:133-143.
4. Bradley K.J., Bowl M.R., Williams S.E., Ahmad B.N., Partridge C.J., Patmanidi A.L., Kennedy A.M., Loh N.Y., Thakker R.V. Parafibromin is a nuclear protein with a functional monopartite nuclear localization signal. Oncogene 2007, 26:1213-1221.
5. Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974, 77:71-94.
6. Carpten J.D., Robbins C.M., Villablanca A., Forsberg L., Presciuttini S., Bailey-Wilson J., Simonds W.F., Gillanders E.M., Kennedy A.M., Chen J.D., Agarwal S.K., Sood R., Jones M.P., Moses T.Y., Haven C., Petillo D., Leotlela P.D., Harding B., Cameron D., Pannett A.A., Hoog A., Heath H., James-Newton L.A., Robinson B., Zarbo R.J., Cavaco B.M., Wassif W., Perrier N.D., Rosen I.B., Kristoffersson U., Turnpenny P.D., Farnebo L.O., Besser G.M., Jackson C.E., Morreau H., Trent J.M., Thakker R.V., Marx S.J., Teh B.T., Larsson C., Hobbs M.R. HRPT2, encoding parafibromin, is mutated in hyperparathyroidism-jaw tumor syndrome. Nat. Genet. 2002, 32:676-680.
7. Cassata G., Shemer G., Morandi P., Donhauser R., Podbilewicz B., Baumeister R. ceh-16/engrailed patterns the embryonic epidermis of Caenorhabditis elegans. Development 2005, 132:739-749.
8. Chang M., French-Cornay D., Fan H.Y., Klein H., Denis C.L., Jaehning J.A. A complex containing RNA polymerase II, Paf1p, Cdc73p, Hpr1p, and Ccr4p plays a role in protein kinase C signaling. Mol. Cell. Biol. 1999, 19:1056-1067.
9. Chen Y., Yamaguchi Y., Tsugeno Y., Yamamoto J., Yamada T., Nakamura M., Hisatake K., Handa H. DSIF, the Paf1 complex, and Tat-SF1 have nonredundant, cooperative roles in RNA polymerase II elongation. Genes Dev. 2009, 23:2765-2777.
10. Chin-Sang I.D., Chisholm A.D. Form of the worm: genetics of epidermal morphogenesis in C. elegans. Trends Genet. 2000, 16:544-551.
11. Chu X., Qin X., Xu H., Li L., Wang Z., Li F., Xie X., Zhou H., Shen Y., Long J. Structural insights into Paf1 complex assembly and histone binding. Nucleic Acids Res. 2013, 41:10619-10629. http://dx.doi.org/10.1093/nar/gkt819.
12. Ding L., Paszkowski-Rogacz M., Nitzsche A., Slabicki M.M., Heninger A.K., de Vries I., Kittler R., Junqueira M., Shevchenko A., Schulz H., Hubner N., Doss M.X., Sachinidis A., Hescheler J., Iacone R., Anastassiadis K., Stewart A.F., Pisabarro M.T., Caldarelli A., Poser I., Theis M., Buchholz F. A genome-scale RNAi screen for Oct4 modulators defines a role of the Paf1 complex for embryonic stem cell identity. Cell Stem Cell 2009, 4:403-415.
13. Diogon M., Wissler F., Quintin S., Nagamatsu Y., Sookhareea S., Landmann F., Hutter H., Vitale N., Labouesse M. The RhoGAP RGA-2 and LET-502/ROCK achieve a balance of actomyosin-dependent forces in C. elegans epidermis to control morphogenesis. Development 2007, 134:2469-2479.
14. Edgar L.G., Wolf N., Wood W.B. Early transcription in Caenorhabditis elegans embryos. Development 1994, 120:443-451.
15. Firestein B.L., Rongo C. DLG-1 is a MAGUK similar to SAP97 and is required for adherens junction formation. Mol. Biol. Cell 2001, 12:3465-3475.
16. Gally C., Wissler F., Zahreddine H., Quintin S., Landmann F., Labouesse M. Myosin II regulation during C. elegans embryonic elongation: LET-502/ROCK, MRCK-1 and PAK-1, three kinases with different roles. Development 2009, 136:3109-3119.
17. Hahn M.A., Marsh D.J. Identification of a functional bipartite nuclear localization signal in the tumor suppressor parafibromin. Oncogene 2005, 24:6241-6248.
18. He Y., Doyle M.R., Amasino R.M. PAF1-complex-mediated histone methylation of FLOWERING LOCUS C chromatin is required for the vernalization-responsive, winter-annual habit in Arabidopsis. Genes Dev. 2004, 18:2774-2784.
19. Jaehning J.A. The Paf1 complex: platform or player in RNA polymerase II transcription?. Biochim. Biophys. Acta 2010, 1799:379-388.
20. Kim J., Guermah M., Roeder R.G. The human PAF1 complex acts in chromatin transcription elongation both independently and cooperatively with SII/TFIIS. Cell 2010, 140:491-503.
21. Kim K.Y., Levin D.E. Mpk1 MAPK association with the Paf1 complex blocks Sen1-mediated premature transcription termination. Cell 2011, 144:745-756.
22. Kostas S.A., Fire A. The T-box factor MLS-1 acts as a molecular switch during specification of nonstriated muscle in C. elegans. Genes Dev. 2002, 16:257-269.
23. Labouesse M. Role of the extracellular matrix in epithelial morphogenesis: a view from C. elegans. Organogenesis 2012, 8:65-70.
24. Landmann F., Quintin S., Labouesse M. Multiple regulatory elements with spatially and temporally distinct activities control the expression of the epithelial differentiation gene lin-26 in C. elegans. Dev. Biol. 2004, 265:478-490.
25. Langenbacher A.D., Nguyen C.T., Cavanaugh A.M., Huang J., Lu F., Chen J.N. The PAF1 complex differentially regulates cardiomyocyte specification. Dev. Biol. 2011, 353:19-28.
26. Lin L., Zhang J.H., Panicker L.M., Simonds W.F. The parafibromin tumor suppressor protein inhibits cell proliferation by repression of the c-myc proto-oncogene. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:17420-17425.
27. Lynch A.M., Hardin J. The assembly and maintenance of epithelial junctions in C. elegans. Front. Biosci. 2009, 14:1414-1432.
28. Maduro M., Pilgrim D. Identification and cloning of unc-119, a gene expressed in the Caenorhabditis elegans nervous system. Genetics 1995, 141:977-988.
29. Maduro M., Pilgrim D. Conservation of function and expression of unc-119 from two Caenorhabditis species despite divergence of non-coding DNA. Gene 1996, 183:77-85.
30. Maeda I., Kohara Y., Yamamoto M., Sugimoto A. Large-scale analysis of gene function in Caenorhabditis elegans by high-throughput RNAi. Curr. Biol. 2001, 11:171-176.
31. Magdolen V., Lang P., Mages G., Hermann H., Bandlow W. The gene LEO1 on yeast chromosome XV encodes a non-essential, extremely hydrophilic protein. Biochim. Biophys. Acta 1994, 1218:205-209.
32. Mello C.C., Kramer J.M., Stinchcomb D., Ambros V. Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 1991, 10:3959-3970.
33. Michaux G., Legouis R., Labouesse M. Epithelial biology: lessons from Caenorhabditis elegans. Gene 2001, 277:83-100.
34. Moniaux N., Nemos C., Schmied B.M., Chauhan S.C., Deb S., Morikane K., Choudhury A., Vanlith M., Sutherlin M., Sikela J.M., Hollingsworth M.A., Batra S.K. The human homologue of the RNA polymerase II-associated factor 1 (hPaf1), localized on the 19q13 amplicon, is associated with tumorigenesis. Oncogene 2006, 25:3247-3257.
35. Mosimann C., Hausmann G., Basler K. Parafibromin/Hyrax activates Wnt/Wg target gene transcription by direct association with beta-catenin/Armadillo. Cell 2006, 125:327-341.
36. Mosimann C., Hausmann G., Basler K. The role of Parafibromin/Hyrax as a nuclear Gli/Ci-interacting protein in Hedgehog target gene control. Mech. Dev. 2009, 126:394-405.
37. Mueller C.L., Jaehning J.A. Ctr9, Rtf1, and Leo1 are components of the Paf1/RNA polymerase II complex. Mol. Cell. Biol. 2002, 22:1971-1980.
38. Mueller C.L., Porter S.E., Hoffman M.G., Jaehning J.A. The Paf1 complex has functions independent of actively transcribing RNA polymerase II. Mol. Cell 2004, 14:447-456.
39. Nguyen C.T., Langenbacher A., Hsieh M., Chen J.N. The PAF1 complex component Leo1 is essential for cardiac and neural crest development in zebrafish. Dev. Biol. 2010, 341:167-175.
40. Oh S., Zhang H., Ludwig P., van Nocker S. A mechanism related to the yeast transcriptional regulator Paf1c is required for expression of the Arabidopsis FLC/MAF MADS box gene family. Plant Cell 2004, 16:2940-2953.
41. Patel F.B., Bernadskaya Y.Y., Chen E., Jobanputra A., Pooladi Z., Freeman K.L., Gally C., Mohler W.A., Soto M.C. The WAVE/SCAR complex promotes polarized cell movements and actin enrichment in epithelia during C. elegans embryogenesis. Dev. Biol. 2008, 324:297-309.
42. Piekny A.J., Johnson J.L., Cham G.D., Mains P.E. The Caenorhabditis elegans nonmuscle myosin genes nmy-1 and nmy-2 function as redundant components of the let-502/Rho-binding kinase and mel-11/myosin phosphatase pathway during embryonic morphogenesis. Development 2003, 130:5695-5704.
43. Ponnusamy M.P., Deb S., Dey P., Chakraborty S., Rachagani S., Senapati S., Batra S.K. RNA polymerase II associated factor 1/PD2 maintains self-renewal by its interaction with Oct3/4 in mouse embryonic stem cells. Stem Cells 2009, 27:3001-3011.
44. Porter S.E., Washburn T.M., Chang M., Jaehning J.A. The yeast pafl-rNA polymerase II complex is required for full expression of a subset of cell cycle-regulated genes. Eukaryot. Cell 2002, 1:830-842.
45. Praitis V., Casey E., Collar D., Austin J. Creation of low-copy integrated transgenic lines in Caenorhabditis elegans. Genetics 2001, 157:1217-1226.
46. Priess J.R., Hirsh D.I. Caenorhabditis elegans morphogenesis: the role of the cytoskeleton in elongation of the embryo. Dev. Biol. 1986, 117:156-173.
47. Rozenblatt-Rosen O., Hughes C.M., Nannepaga S.J., Shanmugam K.S., Copeland T.D., Guszczynski T., Resau J.H., Meyerson M. The parafibromin tumor suppressor protein is part of a human Paf1 complex. Mol. Cell. Biol. 2005, 25:612-620.
48. Rozenblatt-Rosen O., Nagaike T., Francis J.M., Kaneko S., Glatt K.A., Hughes C.M., LaFramboise T., Manley J.L., Meyerson M. The tumor suppressor Cdc73 functionally associates with CPSF and CstF 3' mRNA processing factors. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:755-760.
49. Shi X., Chang M., Wolf A.J., Chang C.H., Frazer-Abel A.A., Wade P.A., Burton Z.F., Jaehning J.A. Cdc73p and Paf1p are found in a novel RNA polymerase II-containing complex distinct from the Srbp-containing holoenzyme. Mol. Cell. Biol. 1997, 17:1160-1169.
50. Shi X., Finkelstein A., Wolf A.J., Wade P.A., Burton Z.F., Jaehning J.A. Paf1p, an RNA polymerase II-associated factor in Saccharomyces cerevisiae, may have both positive and negative roles in transcription. Mol. Cell. Biol. 1996, 16:669-676.
51. Simske J.S., Hardin J. Getting into shape: epidermal morphogenesis in Caenorhabditis elegans embryos. Bioessays 2001, 23:12-23.
52. Sulston J.E., Schierenberg E., White J.G., Thomson J.N. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 1983, 100:64-119.
53. Tenney K., Gerber M., Ilvarsonn A., Schneider J., Gause M., Dorsett D., Eissenberg J.C., Shilatifard A. Drosophila Rtf1 functions in histone methylation, gene expression, and Notch signaling. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:11970-11974.
54. Tomson B.N., Arndt K.M. The many roles of the conserved eukaryotic Paf1 complex in regulating transcription, histone modifications, and disease states. Biochim. Biophys. Acta 2013, 1829:116-126.
55. Totong R., Achilleos A., Nance J. PAR-6 is required for junction formation but not apicobasal polarization in C. elegans embryonic epithelial cells. Development 2007, 134:1259-1268.
56. Toya M., Iida Y., Sugimoto A. Imaging of mitotic spindle dynamics in Caenorhabditis elegans embryos. Methods Cell Biol. 2010, 97:359-372.
57. Toya M., Terasawa M., Nagata K., Iida Y., Sugimoto A. A kinase-independent role for Aurora A in the assembly of mitotic spindle microtubules in Caenorhabditis elegans embryos. Nat. Cell Biol. 2011, 13:708-714.
58. Wade P.A., Werel W., Fentzke R.C., Thompson N.E., Leykam J.F., Burgess R.R., Jaehning J.A., Burton Z.F. A novel collection of accessory factors associated with yeast RNA polymerase II. Protein Expression Purif. 1996, 8:85-90.
59. Williams-Masson E.M., Heid P.J., Lavin C.A., Hardin J. The cellular mechanism of epithelial rearrangement during morphogenesis of the Caenorhabditis elegans dorsal hypodermis. Dev. Biol. 1998, 204:263-276.
60. Williams-Masson E.M., Malik A.N., Hardin J. An actin-mediated two-step mechanism is required for ventral enclosure of the C. elegans hypodermis. Development 1997, 124:2889-2901.
61. Wissmann A., Ingles J., McGhee J.D., Mains P.E. Caenorhabditis elegans LET-502 is related to Rho-binding kinases and human myotonic dystrophy kinase and interacts genetically with a homolog of the regulatory subunit of smooth muscle myosin phosphatase to affect cell shape. Genes Dev. 1997, 11:409-422.
62. Yart A., Gstaiger M., Wirbelauer C., Pecnik M., Anastasiou D., Hess D., Krek W. The HRPT2 tumor suppressor gene product parafibromin associates with human PAF1 and RNA polymerase II. Mol. Cell. Biol. 2005, 25:5052-5060.
63. Yochem J., Gu T., Han M. A new marker for mosaic analysis in Caenorhabditis elegans indicates a fusion between hyp6 and hyp7, two major components of the hypodermis. Genetics 1998, 149:1323-1334.
64. Zhang C., Mejia L.A., Huang J., Valnegri P., Bennett E.J., Anckar J., Jahani-Asl A., Gallardo G., Ikeuchi Y., Yamada T., Rudnicki M., Harper J.W., Bonni A. The X-linked intellectual disability protein PHF6 associates with the PAF1 complex and regulates neuronal migration in the mammalian brain. Neuron 2013, 78:986-993.
65. Zhang H., Labouesse M. Signalling through mechanical inputs: a coordinated process. J. Cell Sci. 2012, 125:3039-3049.
66. Zhang K., Haversat J.M., Mager J. CTR9/PAF1c regulates molecular lineage identity, histone H3K36 trimethylation and genomic imprinting during preimplantation development. Dev. Biol. 2013, 383:15-27.
67. Zhu B., Mandal S.S., Pham A.D., Zheng Y., Erdjument-Bromage H., Batra S.K., Tempst P., Reinberg D. The human PAF complex coordinates transcription with events downstream of RNA synthesis. Genes Dev. 2005, 19:1668-1673.
68. Zhu B., Zheng Y., Pham A.D., Mandal S.S., Erdjument-Bromage H., Tempst P., Reinberg D. Monoubiquitination of human histone H2B: the factors involved and their roles in HOX gene regulation. Mol. Cell 2005, 20:601-611.